Sensory Evolutionhttps://ecomorph.wordpress.com
the eyes have itWed, 29 Aug 2018 04:27:32 +0000enhourly1http://wordpress.com/https://secure.gravatar.com/blavatar/a4b1f7ca102da628da80e34d16a1e733?s=96&d=https%3A%2F%2Fs0.wp.com%2Fi%2Fbuttonw-com.pngSensory Evolutionhttps://ecomorph.wordpress.com
Sampling strategy and evolutionary transitionshttps://ecomorph.wordpress.com/2017/08/10/sampling-strategy-and-evolutionary-transitions/
Thu, 10 Aug 2017 18:44:19 +0000http://ecomorph.wordpress.com/?p=1168Continue reading →]]>Earlier this year, we published an article on eye size evolution of early tetrapods in PNAS. Dan-Eric Nilsson wrote a very nice commentary on the paper in Current Biology, and we followed up with some clarification concerning our sampling scheme. To further illustrate our point, we prepared an additional figure, which can’t be posted as part of our comment, and hence we are making it available here.

Our point is centered on the idea that the further away one samples from a given transition that represents a release from constraint, the higher the possibility that other factors dilute the signal of that release from constraint. For that reason, we were careful to sample around the water to land transition as narrowly as possible. With this narrow phylogenetic bracket, we try to make the ecological situation of these animals comparable. To understand this point, consider the following figure below.

We wanted to determine how the transition from vision through water to vision through air (a release of constraint) affects eye size evolution and visual ecology of early tetrapods. That particular transition is indicated by the red branch in the phylogeny in the above figure. To understand the influence of this release of constraint on eye size evolution, the phylogeny dictates the sampling of very closely related species from just prior and just after that transition. We highlight candidate taxa with orange and red circles. Ideally, one would sample all species that document this transition, but, especially in the fossil record, that is often impossible.

Note that in our hypothetical example, taxa with vision through air from just after the transition (red circles) have slightly larger eyes than their close relatives that still see through the limiting water medium (orange circles). Now let’s assume one would sample with a much wider phylogenetic bracket, across the phylogeny of all vertebrates. In this case, many other factors known to affect eye size evolution would diminish the signal of the transition from water to land. For example, more distantly related taxa may occupy deep sea habitats (purple), fly in open habitats (green), or don’t even rely on vision anymore (brown). The possible outcome of sampling too broadly is that the true signal is no longer discernible. Only by narrowly examining the transition one can determine the correct pattern of eye size evolution.

Considering the importance of sight for most vertebrate organisms in both food foraging and predator evasion, it can be difficult to conceptualize the idea of an evolutionary shift towards blindness. This difficulty may be because vision is seen as one of the primary sensory mechanisms for engaging in an environment. Even many aquatic animals have specialized eyes, most likely due to the increased difficulty that comes with underwater vision. Consequently, one might expect that most highly developed eyes belong to organisms that live in habitats that are not conducive to vision. However, this hypothesis has not necessarily been supported by evidence. In fact, studies have shown that many animals native to environments that are difficult to navigate visually have instead lost the ability to see entirely, in exchange for alternate means of sight that are more energetically favorable.

One such curious case in the world of evolution is the loss of eyes in the Mexican blind cave fish, Astyanax mexicanus. These fish are native to underwater caves in northeastern Mexico, and are found in completely dark environments (Yoshizawa et al., 2012). The limited amount of light, in addition to the underwater environment, has pushed natural selection towards an alternate means of “sight.”

These effects have been compound so greatly over time that the physical eye structure has been almost entirely eradicated (Figure 1). Alternatively, the Mexican blind cave fish have been shown to possess genes that produce mechanisms that are sensitive to water pressure and object vibrations; the acquisition of these genes may be directly correlated to the loss of their eyes. (Yoshizawa et al., 2012). This is because evolution tends to favor the more efficient option, rather than put resources towards redundant or unnecessary functions; and having two mechanisms for navigation around their environment is very metabolically

Members of academia who specialize in eye regression of the blind cave fish, A. mexicanus, have examined several key genes that control how it forages to determine how the genes function on a molecular level. One of the first genes attributed to eye degeneration codes for a protein called Sonic Hedgehog (SHH).

Much like an engineer who wires together components of a functioning computer, SHH is one of the organizing molecules that help specifically wire neurons in the brain during the embryonic stage of development (Menuet et al., 2007). Expansion of SHH signaling results in super-active genes that lead to lens apoptosis (i.e., programmed cell death) and interrupted eye growth (Yamamoto, Stock, Jeffery, 2004). Simply put, the cells of the lens die and the eye ceases to continue developing.

The blind A. mexicanus has been found to express this gene more than their non-blind counterparts, leading scientists to believe that this gene must have a significant role in eye reduction.

In order to test for a correlation, researchers overexpressed SHH to determine the physiological and genetic effects of the gene. It was observed that A. mexicanus with higher amounts of SHH had overall smaller eye-forming structures, such as the retina, lens, and optic cup (Yamamoto, Stock, and Jeffery, 2004). The adult fish were missing eyes and were unresponsive to light (Yamamoto, Stock, and Jeffery, 2004).

In another study, SHH was also mapped on the genome at varying stages of embryonic development, and it was found that the gene was not transient, but rather well-maintained and spread out to new locations, suggesting that SHH could also be correlated to other factors of brain development that have yet to be explored (Menuet et al., 2007).

The reverse of this process, decrease or inhibition of SHH, was also examined to further confirm correlation. The SHH gene activity was reduced using a drug called Embryos from the A. mexicanus cave-fish were treated with cyclopamine, and these fish had larger eye structures overall (Yamamoto, Stock, and Jeffery, 2004). This supported partial restoration of eye development, however sight was not entirely restored. This is most likely because the cyclopamine was administered either too late or too early into the cave-fish’s embryonic development, minimizing its efficacy (Yamamoto, Stock, and Jeffery, 2004).

More recent research has led studies to focus on a different gene, VAB, which may also explain why the inhibition of SHH did not fully restore eyesight (Yoshizawa et al., 2012). VAB refers to vibration attraction behavior, which allows blind A. mexicanus to sense, locate, and swim towards oscillating objects. VAB is mediated by the number and size of sensory receptors known as cranial superficial neuromasts (SN) in the brain. It is considered an adaptive trait in cave-fish since it improves foraging ability in dim habitats with little food and no large predators (Yoshizawa et al., 2012).

In this particular study, the researchers utilized a genetic analysis of VAB and eye size in blind A. mexicanus whose SN in the eye orbit have been surgically removed, and those with their SN intact (Yoshizawa et al., 2012). It was affirmed that VAB and eye size are strongly correlated with superficial neuromasts located in the eye area, as results showed a significant reduction of VAB when SN were removed.

The genes that control VAB, SN, and eye size were then located and mapped on the complete A. mexicanus genome. It was found that the genome contained 27 linkage groups (LG) containing various genes that could possibly account for VAB, SN, and eye size. Linkage groups refer to groups of genes that act and are inherited as a unit, rather than independently.

These LG were analyzed via quantitative trait locus (QTL) analysis; in this case, meaning that scientists looked at each linkage group to determine which is most likely to be responsible for the three aforementioned traits. The analysis showed a strong correlation between eye loss (eye size) and the VAB sensory system (VAB and SN), supporting the hypothesis that evolution has selected for the VAB sensory system as an adaptive behavior at the expense of eyes (Yoshizawa et al., 2012). This result can be seen as the result of “indirect selection” since eye structures were the trade-off to having the advantage of VAB.

There is a fair amount of evidence supporting the correlation of specific genes to the loss of sight and eye structure entirely in the A. mexicanus. At this point is seems fair to say that sight is a redundant and unnecessary function for these cave-dwelling fish, as they reside in a very dimly-lit environment and they are underwater. One would infer that alternative methods to sensory perception have been developed because blind A. mexicanus with these phenotypes are better adapted to the environment, and more effectively able to forage for food.

Figure 3. A proposed scenario for adaption to cave life mediated by VAB. Droplets of water potentially caused by prey produce ripples and vibrations in the water that blind cave-fish can sense and locate. (from Yoshizawa and Jeffrey, 2011).

However, the actual benefits of eye regression in cave animals have yet to be confirmed. The primary theory is that eye degeneration is metabolically more efficient. It takes a lot of resources to develop and power eyes, as well as put energy towards an alternate method of sight. One might argue that it is just as costly to have eyes and no VAB or SHH, as it is to have VAB or SHH and no eyes. This hypothesis brings us full circle as it brings back the point that, perhaps, the sightless method of vision is a better mechanism than having true eyes. With this in mind, future research has many paths to take and many new questions to answer.

What are the exact metabolic costs of eyes? How do the costs differ from alternative means of sight? Under what conditions are eyes no longer a practical investment? These are important and relevant questions that bring us closer to understanding the complexity of evolution, and potentially to predicting future directions of evolution based on environmental influences.

Yoshizawa, Masato, and William R. Jeffrey. A diagrammatic summary of the enhancement of VAB and SN during adaptation of Astyanax to life in caves. Digital image. National Center for Biotechnology Information. U.S. National Library of Medicine, Jan.-Feb. 2011. Web. 27 May 2017.

Vision is an essential part of many animals’ lives. Smaller animals often rely on vision and fast reaction times to get away from predators and avoid being easy prey. This is true especially in smaller fish, whose lives depend on their ability to quickly recognize a threat and avoid it. Because of the increase in carbon emissions as a product of industrialization, the carbon dioxide (CO2) levels of both air and water are steadily increasing (Figure 1), which has affected fish sensory systems, affecting their abilities to avoid being easy prey.

Figure 1: The estimated increase in CO2 levels in the atmosphere, and the projected impact on the ocean’s pH (McNeil, Matear 2006, Figure 1).

As the ocean takes up CO2, the pH of the water decreases, resulting in a more acidic environment (McNeil, Matear 2006). And with increased CO2 present, fish are unable to perceive their environment correctly. In previous studies, fish were exposed to environments with CO2 levels equivalent to the estimated CO2 levels that will be reached in the near future. It has been found that fishes’ olfactory systems and decision making skills have been detrimentally influenced by CO2, which can result in unfavorable behavior in hazardous situations (Munday, et al. 2008). The diminished sensory perception can result in a lack of discrimination in predatory-prey situations (Allan, et al. 2013), with harmful effects on marine life and behavior.

It’s been theorized that previously observed changes in the behavior and sensory systems in fish can be linked to CO2 interfering with neurotransmitters. You may wonder, how could CO2 influence neurotransmitters at the retinal level?

Neurons transmit visual signals from the photoreceptors to the optic nerve and by extension, the brain (Figure 3), and many connections in between neurons are made by synapses. To get the signal across synapses, neurotransmitters, or chemical messengers, are critically important. The binding of neurotransmitters on receptors across the synapse leads to the opening of channels on the neuron’s membrane and causes the continued propagation of signals (action potentials) on the neuron across the synapse. So, if the concentration of CO2 in the retina is increased by virtue of diffusion from the ambient environment into the eye, the signal transfer from photoreceptors to the brain may be affected (Figure 3).

Chung et al. investigated how CO2 levels alter the neurotransmitter, GABA, and its receptors which are located in the eye. GABA is an “inhibitory” neurotransmitter, so when it binds to receptors on a neuron, it actually stops the neuron from firing. This is counterintuitive because usually neurotransmitters activate neurons, but GABA is used to keep neurons from becoming overstimulated and is useful in controlling activation (this video explains how the neurotransmitter GABA works). The researchers focus on the GABAA receptor because these receptors are present in the eye and would be most likely to be affected by the rising CO2 levels in water (Mora-Ferrer and Neumeyer 2009). In the context of this paper, we are not concerned with how GABA is formed, but rather we are concerned with its function as an “inhibitory” neurotransmitter.

In the experiment, Chung and colleagues investigated the ability of these damselfish to differentiate between flickering light and constant light. This ability is important because it’s a measure for how well they can resolve super quickly changing scenes, such as rapid movements of predators. When the light flickered, the researchers examined changes in the eye at the retinal level, measuring the eye’s chemical responses by using an electrode placed on the eye. Eventually, the flickering occurred so fast that the fish was unable to tell whether or not the light was continuous, and thus no chemical response was produced (Figure 4). This was referred to as the fish’s CFF threshold, or “critical flicker fusion threshold” (Chung, et al. 2014). The threshold differs from fish to fish depending on its circadian rhythm and lighting in its natural environment, but for this experiment Chung et al. focused mainly on the threshold values of the spiny damselfish.

Figure 4. The critical flicker fusion frequency is reached when the light flickers so fast that it appears as a continuous light.

They found each damselfish’s threshold by immobilizing the fish on a plastic board and covering one of its eyes. They placed an electrode on the uncovered eye (which was exposed to air) and flashed a light at the fish. From the signals measured, the researchers found that when the fish were kept in water with CO2 levels equal to levels that the ocean is estimated to reach by the year 2100, their CFF threshold values significantly decreased. This means their ability to see worsened substantially. This could affect the survivability of a fish, impairing its ability to quickly recognize harmful situations and avoid capture by predators.

For the second part of the experiment, the researchers sought to examine whether or not it was truly GABAA receptors being influenced by the increasing acidification of the environment. They treated the fish with GABA antagonists and ran the same trials to test their thresholds. An antagonist is a chemical that binds to neurotransmitter receptors to prevent neurotransmitters from binding to these receptors. Antagonists share highly similar molecular structures to the neurotransmitter that the receptor normally binds with, and is therefore able to bind to these receptors in order to reduce the effects of a neurotransmitter by blocking the receptors. In this case, a GABA antagonist would reverse the effects of GABA and in turn cause more neural stimulation because it stops GABA’s ability to reduce a neuron’s ability to send signals.

In addition to the reversal effects of the GABA antagonist, researchers also found that the length of exposure to the GABA antagonist was correlated to the extent of the reversal (Figure 4). When introduced to the GABA antagonist for 20 minutes, the CFF threshold of the fish in elevated CO2 water increased significantly and became closer to normal. These findings are in conjunction with knowing that when GABA binds to its receptors, it stops neurons from firing, so with lower levels of GABA binding, the neurons in the eye will activate more. This GABA decrease would allow the fish to react to stimuli more quickly and be able to identify more changes in their environment. Although the thresholds for the fish in normal water also increased slightly when GABA antagonists were added, this change was not statistically significant.

Figure 5. Using GABA antagonists, the thresholds of fish exposed to high levels of CO2 can increase. This graph shows the thresholds of fish in normal water (triangles) and fish in water with high CO2 levels (squares). The fish were introduced to GABA antagonists at time zero. (Chung, et al. 2014, Figure 1)

Chung and colleagues convincingly demonstrate how ocean acidification decreases the ability of fish to resolve sudden visual changes. What they don’t discuss yet is how we could go about counteracting the effects of ocean acidification, should it reach the predicted levels in Figure 1, but it’s a distressing possibility that is recognized as a very big issue and is being researched. Further research should also investigate how GABAA receptors are actually changed by ocean acidification or how the brain itself may be affected, as the authors mention. Another important topic to look into is how high CO2 levels affect GABAA receptors in all fish, not just this specific species of damselfish.

To conclude, the above example delves into a real-world consequence of global warming. By showing that damselfish were not able to react to stimuli as well or quickly when exposed to acidified water, this research is further evidence that unless we cut down on carbon and fossil fuel emissions and slow the acidification of the ocean, it’s likely that the sensory systems and behavior of fish will begin to endure harmful effects. This sensory deprivation could likely result in a decrease of the fitness of affected species and even extinction, reversing millions of years of evolution and mutations because of their inability to react in dangerous environments. Larger devastation up and down the food chain may occur, unless species have sufficient time to adapt to the impending threats. These adaptations could take hundreds of years to occur and it’s unknown if the damselfish would survive long enough.

In the vast expanse of the aquatic realms, certain fish have evolved a truly “shocking” sensory system. For a second, imagine that you are walking down the street. Then, out of nowhere, you feel someone running up behind you. But, you can’t hear, see, or smell them. Instead, you sense them based on the disturbance of an electric field around you. If you were an electroreceptive fish, interactions like this would occur on a daily basis.

Gymnotiformes (South American knife fish, Figure 1), represent one of the present day groups of weakly electric fish. For many years, knife fish have been a subject of study due to their unique electroreceptive ability. Gymnotiform fish have the ability to emit an electrical field using a specialized electrical organ (EO) consisting of modified muscle cells, located on their underside (Pedraja et al. 2016). This organ emits wave-like discharges, referred to as Electrical Organ Discharges, or EODs. These EODs are controlled by a section of the gymnotiform brain called the pacemaker nucleus (Salazar et al., 2013). As the name suggests, this set of specialized neurons acts as a control mechanism for the pace of release of EODs, which are then interpreted by channel-like structures on the skin (Figure 2; Salazar et al., 2013). As electrical impulses travel through the channels on the highly conductive skin, they are interpreted by the pacemaker nucleus and its supporting cast, the sublemniscal and central posterior pacemaker nuclei (SPPN and CP respectively), which relay information to different areas of the body surface through which electrical output is delivered (Salazar et al., 2013). These structures dictate the speed and intensity of the EOD, helping knife fish respond to changes in their surroundings quickly and efficiently.

While these weakly electric fish swim, they constantly put out EODs at different rates, and can interpret changes in their own EOD’s to inform themselves about their surroundings. Gymnotiforms come in contact with many different types of organisms and obstacles and are essentially in constant motion. To have a functioning electroreceptive sensory system, they need to constantly adjust their sensory neurons to interpret different stimuli for their electroreception to be effective (Marquez et al., 2013).

In their lab in Uruguay, Pedraja et al. studied the implications of EOD sensing in antagonistic interactions of knife fish. They focused on the role of EODs in aggressive or competitive behavior, as they were curious as to how size difference plays a role in the aggressive behaviors of gymnotiform fish. Much like our own fight or flight syndrome, when gymnotiform fish encounter competitive scenarios, they assess whether or not to act in an aggressive manner to secure territory or resources.

To evaluate how interpretation of size plays a role in these decisions, Pedraja et al. placed two knife fish of different sizes in the same tank, separated by a partition for 2 hours (Figure 2, Panel A; Pedraja et al., 2016). This partition prevented fish from communicating with their contender via electrical signals. Next, the researchers turned off the lights and allowed the fish to acclimate for 10 minutes. Afterwards, the researchers removed the partition and observed the behaviors of the two fish, which couldn’t use any visual signals to evaluate their opponent because of complete darkness. Sizing up their contender had to be done with their electroreception (or possibly with their lateral lines).

To record the unfolding scene, the researchers fitted the electrically isolated enclosure with 2 sets of electrodes on opposite sets of walls. The water was kept at roughly 20 degrees Celsius, which has been found in many other experiments to be ideal for gymnotiform EOD, and the subjects were filmed at 30 FPS from below, with the tank illuminated by infrared light (Pedraja et al., 2016).

The larger fish emerged as the winner in most rounds, showing its dominance by driving away its smaller contender on three consecutive attacks without eliciting a counter strike (Pedraja et al. 2016). If knife fish were capable of assessing the size of their opponent by using their electric sense one might think smaller knife fish wouldn’t pick a fight with a larger contender, but that was not the case. It is of course possible that the very much constrained arena didn’t leave them much of a choice, and behavior in natural habitats may well be different. However, through observations of behavior during interactions and modeling of electric fields Pedraja et al. provide evidence to support that the detection and interpretation of electric fields in antagonistic behaviors plays an important role.

Figure 2: Stills and schematics of the experimental procedure used by Pedraja et al. (2016).

Now, all of this is interesting as it illustrates how electric fields can be used by fish to monitor their surroundings, but you’re probably sitting there reading this, thinking “why does all of this matter to me? I’m not a fish.” Well, the basic principles behind gymnotiform electrolocation have much potential to revolutionize the operation of robotic technology in deep-sea exploration. It is a well-known fact that our exploration of the vast ocean has been all but comprehensive. As of now, our exploration of the vast depths of the oceans is quite limited by the availability of light in deep sea conditions. However, the principles behind gymnotiform electroloction may prove to be useful in expanding our horizons, so to speak. If we could use the same bio-electroreceptive principles utilized by gymnotiforms, it would be possible to have unmanned submarines accurately and thoroughly depict deep-ocean life and the unseen wonders it has to offer (MacIver et al., 2001, 2004).

]]>Figure1_FINALecomorphFigure2_FINALFigure3_FINALNow You See It, Now…Why Do You Need So Many Different Eyes?https://ecomorph.wordpress.com/2017/05/17/now-you-see-it-nowwhy-do-you-need-so-many-different-eyes/
Wed, 17 May 2017 08:07:36 +0000http://ecomorph.wordpress.com/?p=979Continue reading →]]>by Sara E. Freimuth, Claremont McKenna College [edited by Lars Schmitz as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only].

Imagine you have more than just the two eyes on your face – you have eyes on the top of your head, eyes spanning down your arms and resting on each fingertip, an eye or two at your bellybutton, and even eyes on the bottoms of your feet. Now, imagine that with all of these eyes and all that you can see, you are unable to move beyond choosing to sit or stand in the spot you are right now. You’re probably thinking, if I can’t go anywhere, why do I need all these eyes?

What you are imagining is close to what a fan worm – a sessile marine annelid – looks like and experiences throughout its entire lifetime, and what you are probably thinking is what researchers have been wondering for decades: Why do fan worms have so many complex and diverse radiolar eyes if they live such a sedentary life?

With this question in mind, the radiolar eyes of fan worms, or sabellids, make them an excellent case for examining the emergence of novel visual systems, the development of rudimentary visually guided behaviors, and the function of distributed sensory systems (Bok, Capa, and Nilsson, 2016). The diverse and apparently recently evolved array of eyes in fan worms also surprisingly reveal similarities to both arthropods and vertebrates. Thus, while much has been discovered about the anatomy and physiology of the sabellid visual system, there is still a lot to uncover about what has necessitated its complexity and how it came to be.

Fan worms are sessile, tube-dwelling organisms that possess colorful feather-like appendages called radiolar or branchial crowns (Figure 1). They build their protective tubes with mucous secretions, use their radiolar crowns for feeding and respiration, and have a series of segmental bristles that act as a system to help move the fan worms within their tubes and along the sea floor, should they need to abandon their tubes under the most extreme duress.

Despite remaining stationary in their tubes for practically their entire lives, sabellids have a uniquely diverse set of eyes distributed across their entire bodies, and their radiolar eyes, in particular, relate them to other unexpected organisms. While these radiolar eyes, on the one hand, resemble the compound eyes of arthropods in location and function, physiological examination of sabellid radiolar eyes has interestingly related them more closely to vertebrates (Figure 2).

Figure 2. A summary of the currently accepted molecular phylogeny of the “Big Nine” animal phyla that highlights in red the phylum of the fan worm, Annelida, and the phyla with similar visual structures: Arthropoda and subphylum Vertebrata within Chordata. [constructed as summary of Nielsen, 1995]

Michael Bok, María Capa, and Dan-Eric Nilsson explored the physiology of sabellid radiolar eyes through microscopy, and the combination of these results and the review of more than 100 years of investigations into the anatomical diversity and function of sabellid eyes has substantially improved the understanding of sabellid vision in terms of developmental, evolutionary, and functional significance. The culmination of this research, then, has resulted in the organization and classification of sabellid visual structures into more distinct hierarchies with important evolutionary implications. This visual hierarchy of sabellids yields a perplexing complexity.

At the simplest hierarchical level in the classification of any vision are photoreceptors, which are ambient-light sensitive cells and the primary unit of visual systems. Photoreceptors, historically, have been classified by their differing signaling pathways and structures into two distinct realms: rhabdomeric photoreceptors of invertebrates, such as arthropods, molluscs, and annelids, and ciliary photoreceptors of vertebrates (Arendt, 2003).

Figure 3. The photoreceptor A shows the general shape and structure of a rhabdomeric photoreceptor found typically in invertebrates, and the photoreceptor B shows that of a ciliary photoreceptor found typically in vertebrates and sabellids. [Figure 3 from Arendt, 2003]

The photoreceptors of sabellids that compose the elements of their visual system within the protective tube are observed to be rhabdomeric in nature. However, results of physiological investigations of the outer, unprotected eyes – the radiolar eyes – of these annelids classify these photoreceptors as ciliary, contradicting the previously established dichotomy and relating the radiolar parts of the visual system of fan worms more closely to vertebrates than to arthropods or other annelids (Bok, Capa, and Nilsson, 2016).

Next up are the ocelli, basic one-pixel light detectors composed of photoreceptive cells that generate directional light sensitivity but not quite full vision. Sabellids have four main types of ocelli – cerebral, segmental, pygidial, and radiolar – that all exhibit an array of visual capabilities for a variety of functions (Figure 4). The former three are all rhabdomeric and housed within the tube of the fan worm, while the latter are ciliary and in multiple types that ultimately compose radiolar eyes.

Figure 4. A stylized drawing of a sabellid, featuring the various types of ocelli and other notable anatomical features. Radiolar ocelli are unlabeled in this diagram but are included within the radiolar eyes. [Figure 1 from Bok, Cara, and Nilsson, 2016]

The cerebral ocelli, which are buried in the head of the fan worm, typically only have a single rhabdomeric photoreceptive cell, which is reminiscent of arthropods (Bok, Capa, and Nilsson, 2016). Given their location, these cerebral ocelli are useful for little more than metering of ambient light levels. This capability suggests a regulatory function for biological rhythms.

The segmental ocelli also are located within the fan worm tube and consist of two to three rhabdomeric photoreceptors whose illumination invokes a light avoidance response without cerebral input, which suggests these ocelli function to alert the worm that its trunk is exposed.

Even further down in the tube are the pygidial ocelli, which also are of rudimentary rhabdomeric nature and are potentially involved in the quest for a dark location to form a new tube by fan worms that have abandoned their old ones.

The final type of ocelli – radiolar ocelli – populate the radioles of sabellids and consist of four different subtypes classified by their number of cells (Figure 5). Initially, transmission emission microscopy (TEM) found only three types of radiolar ocelli with one, two, and three cells, but Bok, Capa, and Nilsson have used TEM to categorize a fourth type of ocellus with four cells. These researchers even suggest that further investigation of radiolar photoreceptor pigments could yield radiolar ocelli outside these four established realms (Bok, Capa, and Nilsson, 2016).

These different types of radiolar ocelli constitute the various forms of radiolar eyes in sabellids, which are part of the next level in the hierarchy of their visual system. Eyes, more generally speaking, consist of at least a single ocellus elaborated with many photoreceptors or cluster together many ocelli in a localized, ordered array. If elaborate enough, eyes have the potential for true image-forming vision in which different photoreceptors sample different points in space.

The radiolar eyes of sabellids can be classified in four different types of eyes: Type S, Type CP, Type CS, and Type CI (Figure 6). While most radiolar eyes fit easily into these ranks, some do not conform clearly to a single classification, and it is important to note that many species of sabellids possess no obvious radiolar eyes at all (Bok, Capa, and Nilsson, 2016).

Type S eyes are composed of scattered single ocelli and are found on both sides of the outside of radioles. They typically occur on every radiole and are occasionally denser on more dorsal radioles. They are the most variable of radiolar eye types in complexity and thus have three subtypes categorized Sa, Sb, and Sc based on the scattering pattern of the ocelli.

Type CP eyes are compound-paired eyes found in several pairs in multiple positions along the outer margins of each radiole. They vary in their presence and pigmentation among different sabellid species and generally decrease in size and number of facets as they approach the tip of the radiole.

Type CS, or compound-single eyes, are similar in that they, too, lie along the outer margins of the radioles, with several inhabiting each. Their development, however, is unique in that these eyes seem to derive from one side of the radiole and grow towards the center, rather than developing in the center and growing towards the sides.

Lastly, Type CI eyes, or compound-inside eyes, are located on the inner margins of the radioles at the distal tip, finishing off whatever chain of eyes the radiole contains. Type CI eyes, like Type S eyes, also vary greatly but in terms of size and location (Bok, Capa, and Nilsson, 2016).

The single purpose of sabellid eyes for this protective withdrawal response, then, raises a variety of questions. First, this singular purpose potentially suggests that the array of radiolar eyes is not necessarily providing true spatial vision in that the withdrawal response it solicits relies on shadow detection and, thus, may not need to convey any type of image formation by the nervous system. If this is the case, then these eyes only have directional photoreception, rather than true image-forming vision.

A possible explanation to counter this and support true vision is that the neural processing of radiolar visual input in sabellids is more typical of vertebrates than that of other annelids. There are two types of evidence that may support this explanation. First, one radiole drifting into another’s field of vision does not trigger the withdrawal response, which suggests the radiolar eyes can see some level of depth and supports that they have more complex neural pathways and vision that is more complex than just directional photoreception. Additionally, fan worms have the ability to regenerate their branchial crowns if they are partially removed, which also seems indicative of a more complex neural network, or at least one that is easily altered and extremely resilient (Bok, Capa, and Nilsson, 2016). Both these factors suggest unique neural pathways for sabellids which may yield fascinating results with further investigation.

Another question is why sabellids don’t just use two giant compound eyes to trigger this response instead of the spread of so many different little ones. While this more elegant model of two centralized, economical eyes with great vantage points at the tips of radioles has been successful in other organisms, like arthropods, the dispersal of radiolar eyes seems to account for their vulnerability in the sessile sabellid and may have other potential unknown benefits to be discovered with future exploration (Bok, Capa, and Nilsson, 2016).

The final question that remains is how these eyes evolved. Sabellids have been grouped monophyletically by overall morphology pretty conclusively, but the diversity of their eyes represents anything but a single evolutionary progression (Bok, Capa, and Nilsson, 2016). Interestingly enough, the most complex radiolar eye types of fan worms are not formed by the most complex forms of radiolar ocelli either. With this in mind, it is proposed that sabellids are still contained within one monophyletic group, but there were perhaps at least two or three independent emergences of the radiolar ocelli that constitute their eyes, which likely have just been lost in certain subsequent eye-less genera (Bok, Capa, and Nilsson, 2016).

Moreover, the similarities of sabellid visual structures to both arthropods and vertebrates also remain an evolutionary perplexity that could be better understood with a variety of further investigations. Not only could the aforementioned neural analysis answer questions of both evolutionary and functional similarity of radiolar eyes to arthropods and vertebrates, but an investigation of their opsins, proteins that constitute visual pigments which have been classified in groups similar to those formerly differentiated by rhabdomeric and ciliary photoreceptors, could also clarify (or further complicate) things.

Ultimately, the diverse collection of eyes in fan worms and variety of radiolar eyes in particular posit a unique case of a dispersed sensory system. While the current understanding explores these similarities in functional, physiological, and evolutionary terms, further genetic, developmental, and neurological investigation of sabellid radiolar eyes could yield fascinating insights into the evolution of eyes and visually guided behaviors in general (Bok, Capa, and Nilsson, 2016).

When an organism encounters different ecological niches, populations may undergo divergent selection tied to the requirements of each niche. When this occurs, reproductive isolation may take place, eventually resulting in the formation of distinct species (Van Valen, 1976). While this narrative of ecological speciation is well established and makes frequent appearances in biology textbooks, the selective forces that initiate this process are often quite challenging to determine (Maan, Seehausen, and Groothius, 2016). However, studies over the last decade have begun to shed light on the important role that sensory drive may play in speciation. Here I will dive deeper into how exposure to alternative sensory environments, with specific focus on visual conditions, may lead to divergent sensory adaptations and eventual speciation.

What do we already know?

We all know as living creatures that sensory perception is critically important for survival and reproduction. In addition, there are a variety of different sensory environments that animals can inhabit. Non-surprisingly then, there exists a large diversity in sensory systems across the animal kingdom, depending on various navigation, food detection, predator evasion, and mate selection requirements.

Perhaps the most abundant research involving the role of such sensory drive is focused on aquatic environments where heterogeneity in visual conditions is greatly pronounced by changes in water depth and turbidity (Maan, Seehausen, and Groothius, 2016). Cichlids are a family of fish that are known to be among the most species-rich within vertebrates, consisting of approximately 2,000 species (Kocher, 2004)! Certain cichlid lineages, such as haplochromines, have been subject to multiple adaptive radiations, making them a point of interest in speciation research (Salzburger et al., 2005). Previous studies have found that such radiations show considerable variation in color vision traits, which has been correlated to differing visual habitat and sexual selection (Boughman, 2002; Carleton et al., 2005; Maan et al., 2006; Seehausen et al., 2008; Miyagi et al., 2012).

The two haplochromine species that I will be paying special attention to are Pundamilia pundamilia and Pundamilianyererei. These incipient sister species have reached a level in speciation where reproductive isolation has been mostly achieved, but occasional hybridization does occur (Seehausen, 2009). Both are known to inhabit Lake Victoria, a location in Africa where over 500 species of brightly colored cichlids have radiated over a short span of time (Fryer and Iles, 1972). However, P. nyererei lives at greater water depths than P. pundamilia and, therefore, encounters a very different visual environment (Seehausen 2009; Maan, Seehausen, and Groothius, 2016). In the turbid waters of Lake Victoria, light with short wavelengths, such as blue and violet, is absorbed rapidly while longer wavelength light, such as red and yellow, penetrates to greater water depths (Lythgoe, 1984). As a result, the deeper habitat of P. nyererei has a reddish/yellowish spectrum, as compared to the broad daylight spectrum that P. pundamilia experiences. This variation in photic environment has been associated with genetic differences between the two species, resulting in divergent color vision traits and male body color (Carleton et al., 2005). Previous research has found that, due to differences in color vision, P. pundamilia females prefer the jet blue coloration characteristic of P. pundamilia males, while P. nyererei females prefer the red coloration of P. nyererei males (Selz et al., 2014). Such findings demonstrate how sensory drive may play a vital role in the reproductive isolation of these cichlids (Figure 1).

Figure 1. Overview of how sensory drive has contributed to the population divergence and reproductive isolation of P. pundamilia and P. nyererei. Taken from “Sex, speciation, and fishy physics”. Understanding Evolution. University of California Museum of Paleontology. 02 May 2017, http://evolution.berkeley.edu/evolibrary/news/090301_cichlidspeciation.

Measuring fitness

Now that we’ve seen how differences in visual environment can influence sexual selection, let us ask how might it influence survival. A recent study conducted by Maan, Seehausen, and Groothuis addresses a key component of haplochromine speciation that had not yet been researched in terms of sensory drive – fitness. In order to initiate and sustain divergent populations, the adaptations selected for in a given niche most commonly convey some sort of fitness advantage (Maan, Seehausen, and Groothius, 2016). These researchers wanted to see if the adaptations forming in P. pundamilia and P. nyererei actually gave them a greater survival rate within their visual niche. To find out, they set up reciprocal transplant experiments in which groups of P. pundamilia and P. nyererei were reared in shallow light conditions and deep light conditions (Figure 2 & 3). The shallow conditions were made to emulate the natural visual environment of P. pundamilia and the deep conditions resembled the natural visual environment of P. nyererei. In this way, experimenters were able to compare the survival rates between treatments.

Figure 2. Generalized schematic of the reciprocal transplant experimental set-up used by Maan, Seehausen, and Groothius to compare the effect of visual environment on the fitness of P. pundamilia and P. nyererei. Source: Nicole Hourie.

What they found was that both P. pundamilia and P. nyererei did indeed have higher survival rates in the light environment that mimicked their natural habitat (Figure 4). This study therefore provides the first evidence suggesting that the differences in visual perception between these species convey a fitness advantage within the species’ niche. These findings further bolster the notions that 1) the differences in color vision are adaptive and 2) the differences in visual environment are a strong enough force to drive such divergence in visual properties. Not to mention, since the two species used are still in intermediate stages of speciation, the implication can be made that differing visual adaptations play a significant role in the initiation of population divergence.

Figure 4. Survival rate of F1 offspring of P. pundamilia, P. nyererei, and hybrids under light treatments simulating their natural visual environments of Lake Victoria. (Top six panels) Proportion of surviving offspring at 6 and 12 months in the shallow treatment (upper panels) and the deeper treatment (lower panels). Each line/symbol represents a different family. (Bottom two panels) Average proportion of surviving offspring across families. From Maan, Seehausen, and Groothius, 2016.

Let’s get complicated

Their study also compared the survival rates of hybrids in the two light conditions. Here the survival rates did not significantly differ between the visual environments. This makes sense since, in theory, the hybrid represents an intermediate of both parental species (Carleton et al., 2010). Another finding was that the survival rate of hybrids did not significantly differ from that of either parental species in their natural visual habitat. This complicates things a bit. This and previous work has attempted to identify visual environment as the driving force in the speciation of haplochromine cichlids by causing disruptive selection. If this were fully the case, we would expect hybrids to have a lower fitness than either parental species in their natural environment.

For instance, say we have a hybrid and P. nyererei living in the deep habitat treatment. Since P.nyererei has adapted color vision and pigmentation that best suits the light spectrum of deeper waters, we would expect P. nyererei to have a higher survival rate than the hybrid. Because actual results show that the hybrid had a survival rate similar to P. nyererei, we must now consider that differences in visual environment alone may not be enough to cause diverging populations (Maan, Seehausen, and Groothius, 2016). This is not to say that sensory drive does not contribute to speciation whatsoever. What it does mean is that sensory drive may work in conjunction with other ecological factors to facilitate population divergence.

Indeed, other studies have attempted to identify other adaptive divergences involved in the speciation between P. pundamilia and P. nyererei. For instance, a study conducted by Dijkstra, Seehausen, and Metcalfe implicated a divergence in metabolic efficiency and agonistic behavior between the two species as contributing to their speciation. They expected that P. nyererei males would experience a metabolic cost as a result of exhibiting more aggressive behavior (Dijkstra, Seehausen, and Metcalfe, 2013). However, results suggested the opposite – P. nyererei males used less oxygen (for a given body mass) during territorial interactions than P. pundamilia males. Researchers concluded that such findings imply that metabolic efficiency is an adaptation to reduce the cost associated with increased aggression (Dijkstra, Seehausen, and Metcalfe, 2013). However, their results also found that level of territorial aggressiveness did not differ between the two species when placed in social treatments, contradictory to other studies that have observed a heightened aggression in P. nyererei males. While this work hypothesizes that divergence in agonistic behavior and metabolic efficiency may play an important role in the rapid speciation of the haplochromine lineage, it is yet to be substantially supported.

What does this mean for future research?

Undeniably there is a large body of work that implicates sensory adaptations as a major factor of the rapid speciation in the haplochromine lineage. While Mann, Seehausen, and Groothius’s experiment supports the role of sensory drive in cichlid speciation, it also highlights that the entire picture may not yet be fully realized. Continued research must therefore be devoted to identifying any other contributing ecological factors that additionally influence speciation in cichlids.

As more and more scientific research is conducted, we continue to find additional anthropogenic effects on the natural environment and the ecosystems, especially surrounding large metropolitan areas. Besides well-documented anthropogenic processes that affect climate through pollution, emerging data reveal effects on the sensory biology of animals. For example, there is evidence that pollution is hindering animals’ sight and smell. There is evidence that industry and motor vehicle use affect the hearing of animals. But one factor that is just now being researched more is the effect of light pollution on different animals. Specifically, light pollution and other changes to the visual environment can potentially have adverse effects on animal behaviors like camouflage and mate choice.

Urban development has spread widely across almost any land that we can inhabit, and, in a nutshell, artificial light has been an incredible breakthrough for humans. Light has become such a centerpiece for our societies; we see bright and flashy lights prominent wherever humans are present. We have so many lights in such a concentrated area that we are able to see the lights from space (Figures 1 and 2).

Figure 2. Maps of light intensities throughout the United States. Light is one of the most prominent ways how humans alter their environment. [From Swaddle et al. 2015]

Having lights with such intensity is bound to have some effects on animals, and light pollution due to human development is expected to impact the behavior of many animals. According to a recent and very timely essay (Delhey and Peters 2016), human changes to the visual environment can potentially increase predation risk, lead to maladaptive patterns of mate choice, and disrupt mutualistic interactions between pollinators and plants. I want to take this opportunity to highlight some of the important consequences of light pollution on behavior.

Camouflage is an adaptation which relies on animals blending in with their background to remain undetected by potential predators or prey, depending on whether the strategy is not to be seen to avoid being eaten, or not to be seen to strike an ambush attack.

The amount of light in terrestrial environments will alter the way colors are perceived. If a naturally dark environment is lit due to anthropogenic lighting, the camouflage that the organisms use in that environment may become unviable (Swaddle et al. 2015). This will potentially result in an increase in predation on these organisms, exposing them to increased extinction risk. An important issue here is that the change in light intensity through urban development is so sudden that there is not a chance for the organisms to adapt their camouflage on an evolutionary scale before being predated to extinction.

Implications for camouflage may also arise from physically changing the visual environment. Similar to changes in light, changing the environment (the “backdrop”) will make camouflage less viable. As referenced before, camouflage relies on the organism having the specific color and/or pattern to match its background. However, if there is a substantial habitat alteration, with substantial removal of the most commonly found background the animal is trying to blend into, camouflage is essentially useless (Delhey and Peters 2016). While this is not a direct link to light pollution, most environmental degradation happens in or around the metropolis where light pollution is pervasive.

Quite the opposite to camouflage, some organisms have conspicuous, colorful traits which they rely on to communicate with each other and transfer important signals. In tests on cichlid fish it was found that changes in irradiance (ambient light) and transmission properties of water due to increased turbidity had a direct effect on mating behaviors of females (Delhey and Peters 2016, Figure 3). This is potentially problematic because coloration is one way that these fish can differentiate males of their own species from other cichlid species. If female fish attempt to mate with males of another species they will likely not have viable offspring, and may not even be able to mate successfully at all. This could have drastic effects on the fitness of the species as a whole.

Figure 3. Changes of ambient light and the transmission properties of water may change the color perception of fishes, with detrimental effects on mate choice. [From Delhey et al. 2016]

The artificial environment that humans have created is also potentially problematic for the visual perception of organisms. The colors that are used in buildings and even advertisements commonly found in cities have been shown to alter animal behavior (Delhey et al. 2016). For example, pollinators will often seem distracted by and/ or attracted to vibrant colors, which results in a waste of their time and energy. In addition, it is common for people in cities to use their own plants and flowers to decorate their homes and businesses. These flowers draw the attention of pollinators which can result in the native plants having to compete with introduced and invasive species. This can result in lower seed production and thus lower the fitness of the native plant species (Delhey et al. 2016).

Whether it is due to increased lighting or due to changes in environment, changing the visual aspects of an organism’s environment will undoubtedly have an effect on the population. It is likely that potential impacts will include decreases in both population viability and mating success. This is due to the fact that mates will have a hard time recognizing the colors used for reproductive signaling. There will also be the threat of over predation on organisms that typically use camouflage to avoid their predators. The long term population consequences from weakening sexual selection and increasing predation may cause an overall decrease in the fitness of the population.

In order to change this, we must be more aware of the anthropogenic effects on the environment, especially considering light pollution and changes in visual stimulation. More extensive research is needed to proceed with mitigating the effects of anthropogenic light pollution. I think that it would be beneficial to test how animals react to different colors and intensities of light. This would help us to understand possible changes in behavior. In general, with more research we will have a better understanding of how changes in light affect animal behaviors in and around metropolitan areas, leading to better strategies on preventing, or at least decreasing, the impact of light on the environment.

Cave inhabitants, or troglobites, often look very different from their surface dwelling counterparts or even those animals that spend just some of their time underground in the dark. Cave habitats support little life, yet some animals live just fine never seeing the sun, swimming in the eternal darkness of underground lakes and rivers. Often pale, eyeless, and slow moving, many cave species look eerily similar as they coast around in the pitch-black. The morphological continuity of cave species has puzzled scientists for years, but the discovery of a certain species of cavefish in Mexico has provided a genetic key to figuring out what may explain this intriguing pattern. They’re called Astyanax mexicanus, and they’re special because they are relative newcomers to the caves (Figure 1, Krishnan and Rohner, 2016). They appear white, are eyeless and are fully adapted to life in the dark, but they are still genetically similar enough to their surface dwelling relatives that they can interbreed and produce viable offspring.

This suit of characteristics is invaluable to geneticists, because it allows them to pinpoint what genes are involved in traits like eye loss in the fish. A. mexicanus has become a popular model organism for genetic studies on both development and evolution because of their unique traits and genetic malleability (Casane and Rétaux, 2016). When studying cavefish, one question that arises immediately is how they survive without eyes. Most animals we are familiar with use their eyes and sense of sight to find food, mates, and sample their surroundings for dangers, among other things. However, in complete darkness light-dependent eyes are not useful at all. It is apparent that cavefish are still able to survive and reproduce without sight, so the question for research becomes finding out what ultimately caused cavefish to lose their eyes? Was it the evolutionary push to lose eyes simply to save energy, or to make room for other, supercharged, senses that do work in the dark?

Hélène Hinaux and colleagues sought to answer this question, specifically, whether our friend Astyanax mexicanus trades its eyes for a better nose by diverting metabolic energy from eye development into olfactory organs and brain tissue. The research team investigated the development of eyes and olfactory organs in cave and surface fish embryos by looking at several pathways known to be instrumental in the development of the head. These pathways consist of developmental processes linked to a specific chemical receptor or messenger molecule that are often conserved over evolutionary time and therefore popular targets for study. The specific pathways were Sonic hedgehog (Shh), Fibroblast growth factor 8 (FgF8), and Bone morphogenetic protein 4 (Bmp4), all of which are conserved through evolution and therefore play essential roles in development of various parts of the vertebrate head region.

By looking at images of developing fish embryos that had been subjected to several genetic treatments, Hinaux and colleagues discovered how these signaling pathways affect the development of both eyes and olfactory organs (Figure 2, Hinaux et al, 2016).

The development of eyes in cave and surface fish has been studied in depth and is relatively well understood; eyes in both fish morphs begin development the same way, but in cavefish, the cells making up the lens undergo apoptosis and die, initiating developmental differences (Figure 3; Krishnan and Rohner, 2016, Casane and Rétaux, 2016). Before this paper was published, we knew that the regression of eyes in A. mexicanus was caused by evolutionary selective pressures of the cave environment, and was related to the Shh pathway; we also knew that this regression was likely linked to some kind of sensory system trade-off (Yoshizawa et al, 2012).

The actual existence and exact timing of the sensory trade-off event (lens apoptosis), roughly 24 hours after fertilization during the neural plate stage of the fish embryos, was unknown until Hinaux and colleagues published their study (Hinaux et al, 2016). Hinaux and colleagues also further elucidated the mechanisms causing eye-nose trade-off in development of cavefish, by looking at multiple developmental pathways.

Figure 2 (panels F and G from Fig. 5 of Hinaux, et al., 2016). (F) A schematic showing effects of Shh, Fgf8, and Bmp4 signally pathways on the lens and olfactory placodes. (G) Brain placodes (relevant areas of the brain at a set level of development) shown in place in the head, nose at top, with effects of Shh, Fgf8, and Bmp4. Arrows show activation, flat ends show inhibition.

Along with arresting development of the lens and other parts of the eye, cavefish were found to have larger olfactory placodes in their brains and correspondingly larger olfactory organs as they developed when compared to surface fish (Hinaux et al, 2016). This was an exciting discovery because it showed a relatively late determination of brain tissue in developing fish. The olfactory system of cavefish benefits from the loss of eyes, as all three of the pathways studied promote growth of the olfactory placode while leading to the reduction of the lens placode: Fgf8 through heterochrony, Shh through hyper-signaling, and Bmp4 through its absence in the anterior portion of the head, leading to lens placode inactivation (Figure 2, Hinaux et al, 2016). It seems the answer to our earlier question is that the need for a larger and more developed nose pushed energy and resources away from the developing eye towards the nose and its associated brain tissue.

Figure 3 (Fig. 2 from Krishnan and Rohner, 2016). Side by side schematic of eye development in cave and surface fish. Areas affected by Shh shown in blue. Lens apoptosis in cavefish leads to eyeless adults.

After finding this exciting sensory trade-off in development, Hinaux and colleagues tested the olfactory capabilities of cavefish to compare chemical sensitivity between cave and surface fish. By exposing fish to increasingly smaller concentrations of amino acids, specifically alanine and serine, the researchers found the lower limit of the fish’s sense of smell. Their results were astounding; cavefish not only showed much higher olfactory sensitivity than surface fish of the same species, but even gave sharks a run for their money. Cavefish can detect levels of alanine in the water at concentrations as low as 10-10 M (3.36×10-8 grams/gallon) (Figure 4, Hinaux et al, 2016), which is 5 orders of magnitude better than the surface dwellers..

Figure 4 (Fig. 8 from Hinaux et al., 2016). Graphs showing olfactory response and lower limits of cave (CF) and surface (SF) morphs. (A) and (B) shown side by side comparison of amino acid sensitivity of cave and surface fish, (C) shows lower limit for detection of alanine in cavefish. (D) Provides a summary of sensitivity for both morphs.

This supported the hypothesis that cavefish have a better nose than their surface counterparts, and suggests that by losing their eyes, cavefish could devote more energy to developing olfactory organs and tissues. It makes sense that cavefish would need a better sense of smell than surface fish. Any food that the cavefish could subsist on must wash in from outside the cave, since the lack of light in caves inhibits any sort of ecosystem based on photosynthesizing plants or plankton in the water (Casane and Rétaux, 2016). This makes the abundance of edible material in cave water very scarce; a supercharged nose would be extremely useful, and maybe even be essential, to cave living for A. mexicanus. The sensory shift from sight to smell in cavefish is a textbook example of sensory trade-off in the natural world, where shrinkage or complete removal of one sense allows for the betterment of another.

This paper falls into the field of EvoDevo—the fascinating overlap of developmental and evolutionary biology. The results above show how important and surprising this overlap can be. Studying the development of sensory organs in A. mexicanus gives us insight into not only the actual development of cavefish eyes, but also how the loss of eyes and the increased powers of olfaction evolved as the fish ventured into the darkness of caves. Minute changes in developmental signaling pathways must have occurred and proliferated, leading to the evolution of a new subset of the species. Continuing study on A. mexicanus is likely to reveal more interesting ideas on evolution and development, solely because of the possibilities this unique model animal gives us. A. mexicanus has many more secrets to reveal unrelated to its sensory systems; the existence of genetically related, yet geographically isolated, populations of fish present a veritable gold mine of scientific discovery on how one species becomes multiple in real evolutionary time. Stepping away from cavefish, this publication also opens the door to further research on other examples of sensory trade-off, in living species as well as those we learn about through the fossil record.

]]>Figure1ecomorphFigure2Figure3Figure4New insights into the molecular evolution of snake visionhttps://ecomorph.wordpress.com/2017/05/01/snake-vision/
Mon, 01 May 2017 16:48:20 +0000http://ecomorph.wordpress.com/?p=825Continue reading →]]>by: Kennedy A Holland, Claremont McKenna College [edited by Lars Schmitz as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only].

Take a look at the photo below and focus on the unique shape and coloration of the eye.

Figure 1. A green tree python, Morelia viridis, has vertical slits that are common in nocturnal predators. Photo from Thor Hakonsen.

From the thin vertical slit spanning the height of the eye, to the wavelength absorbance patterns in the retina, every detail was selected for through evolution. Whether it concerns hunting strategies, circadian rhythm, or preferred habitat, snake species are incredibly diverse and each are well adapted to their unique niche. There is a growing body of evidence that snakes evolved through a burrowing event from ancestral lizards (Simões et al., 2015). Not only could this have affected the anatomy of the snake, but it may also explain the complexity of snake vision. An alternative hypothesis states that the intense variation in snake species is caused by diurnal and nocturnal differences. So how exactly has vision evolved within snake species that have such different lifestyles? That is the overarching question to which Simões et al. (2016a) set out to find the answer.

Although there have been thorough studies of vision in mammals, fish, and birds, not a lot is known regarding how snake vision evolved or how it changes between various species of snakes.

Let’s go over some background information to gain a basic understanding of snake vision before we dive into the most recent and exciting findings of Simões et al. Snakes are vertebrates, and therefore have vertebrate eyes with photoreceptors that are directed towards the back of the eye (Nilsson, 1996; Figure 2). Already we can see a wide range of eye types in different organisms, but variations do not stop there.

Figure 2. Illustrations of eyes from four different organisms: (a) a vertebrate eye; (b) an arthropod compound eye; (c) a cephalopod lens-eye; (d) a compound eye in polychaete tube-worms and arcoid clams. A snake eye would have the anatomy of eye (a) in this figure. (Nilsson, D. E., 1996).

When light enters the eye, rods and cones in the retina pick up wavelengths and send a signal to the brain via the optic nerve for processing of the image. It has been previously found that snakes have quite variable sets of rod- and cone-like photoreceptors. The amount of diversity within and across snake species is illustrated in Figure 3. Depending on their circadian rhythm, the photoreceptors have evolved and changed shape in response to changes in the snake’s behavior (Simões et al., 2016b). Intuitively, this makes sense, since snakes that are active at night need different vision and light sensitivity than those that are active during the day.

Figure 3. An illustration of the transmutation of cones to rods and vice-versa as explained by Walls, depending on the nocturnal or diurnal behaviors of the snake species. Four varying morphologies of rods and cones within a single species of snake are depicted (Simões et al., 2016b).

Simões et al. investigated the molecular evolution of snake vision, focusing on the three opsin genes present in most snakes: rh1 (rhodopsin), lws (long-wavelength sensitive), and sws1 (short-wavelength sensitive). The researchers performed a large genomic survey of 69 species of snakes. RNA was extracted from the eye, while lenses and spectacles were stored for subsequent spectral transmission measurements. Various visual opsin genes in the DNA were amplified to obtain fragments and later sequenced to be aligned and compared with published sequences from other reptiles and snakes. The alignment was inspected by eye in order to ensure that the nucleotides and amino acids matched properly. Then, multiple branch-model programs and tests provided information that tracked the evolution of sequence changes.

Specifically, the dN/dS test used in this study determined that all opsin genes evolved through purifying selection, indicating strong functional constraints on the molecular evolution of snake vision. Hence, snake vision seems to be suited for for their respective lifestyles.

Previous research on visual opsins has linked shifts in amino acid sites to changes in the maximum wavelength absorbance. From this, it is possible to track the changes in wavelength absorbance over time and find correlations with changes in behavior or lifestyle (Figure 4).

Figure 4. Snake species phylogeny used in analyses of visual opsin gene evolution. The numbers refer to snake clades: (1) Scolecophidia; (2) Alethinophidia; (3) Henophidia; (4) Afrophidia; (5) Caenophidia; (6) Viperidae; (7) Colubridae; (8) Natricinae; (9) Dipsadinae; and (10) Colubrinae. The classifications for ecology (squares) and cell patterns (circles) are shown. Empty circles represent species with unknown states, while strikethrough circles show species with no cones in their retinas. Additionally, findings from experiments with the three visual opsin genes are shown on the right, detailing the UV sensitivity potentials and wavelength absorbances for a specific opsin gene, if present in the snake species. (Simões, B. F. et al., 2016a).

You may have noticed that Figure 4 shows which snake species are ultraviolet sensitive. It is no secret to scientists that many snakes are able to see UV light due to a lens that allows UV wavelengths through, and UVS visual pigments. This study confirms this data, providing further information that the snakes which are UV sensitive are mostly nocturnal, allowing them to see better when foraging at night! Simões et al. concluded that the most recent common ancestor of snakes had UV vision. This is consistent with studies showing the existing trend of UV vision in other nocturnal species. Diurnal species, on the other hand, do not have UV sensitive visual pigments and have lenses that block the UV light from entering the eye. If humans had this feature, we wouldn’t have a need for sunglasses! The removal of UV sensitivity is connected with an increase in acuity and not simply for protection from UV rays. This makes vision for diurnal snakes extra detailed for optimal hunting potential. Furthermore, snakes that hunt during the day tend to absorb slightly longer wavelengths than night active species (Simões et al., 2016a; Figure 5).

Figure 5. Spectral transmission curves are shown for the snakes sampled in this study for (A) lenses and (B) spectacles, including the diurnal or nocturnal tendencies of each species. (C) shows box-plots of wavelengths at which ocular media transmit 50% of the incident illumination (top), and the proportion of UVA transmission (bottom). The box-plots summarize data for the lens (white), spectacle (grey) and a combination of lens and spectacle (black). (Simões, B. F. et al., 2016a).

Although it has been established that the majority of snakes are dichromatic, only seeing two primary colors instead of the three that humans see, trichromacy is speculated to exist in certain species (Davies, W.L., 2009; Simões et al., 2016a). This could be enabled by transmuted cone-like rods for day active snakes, and transmuted rod-like cones in night active snake species (Figure 3). One snake species, the Montpellier snake, only has cones because of its significant diurnal behavior. Additionally, very avid burrowing snake species have lost all of their visual opsins except for rh1 since light sensitivity is more important than color discrimination in dark habitat conditions. This shows that the evolution of snake vision closely matches their hunting behaviors, even at a molecular level, which is fascinating when considering the potential this holds for understanding evolutionary processes in detail.

Walls, back in the 1930’s, came out with the original idea that in saurian eyes, rods and cones can transmute and morph into each other depending on the needs of the species over time (Walls, GL., 1934). Ever since this paper, researchers have supported Walls’ hypothesis by expanding the species studied. Simões et al. have focused on snakes, creating a wider breadth of species that show this pattern of switching rods and cones based on circadian rhythm and hunting strategies. By tracing the changes of specific genes and patterns of rod and cone sets, researchers should be able to establish a phylogenetic history of vision, particularly visual opsin genes. This evolutionary reconstruction can be expanded in future research to provide more information regarding the exact origin of snakes, which remains a question without a definite answer. Although often overlooked in vertebrate studies, snakes are an important addition to the investigation of vision evolution and should continue to be studied moving forward.

Figure 1. An example of the functionality of Retina. Panel (a) shows a simplified outline and the sampling locations of a retinal wholemount. Panel (b) shows the reconstructed map, while (c) illustrates the fit error of the model. [Figure 1 of Cohn et al. 2015, Journal of Vision]

Retinal topography maps are a very widely used tool in visual ecology, as they summarize important information about the distribution of different cell types across the entire retina. These cells can be photoreceptors or ganglion cells, among others, and such cells have often very different densities across the retinal hemisphere. Humans, for example, have one very specialized area with lots of photoreceptors and ganglion cells, the fovea, whereas the peripheral parts of the eye have far less cells. Importantly, these high-density areas correlate with visual acuity. Other species feature very different distribution of cells in the retina, sometimes multiple peaks, or a streak, or a combination of different features. A good taste of the diversity of retinal topographies across vertebrates can be found here, with hundreds of examples.

A major idea and research approach in the field of visual ecology is to link the diversity of retinal topographies to the lifestyle of organisms. And this is what I originally set out to do as part of my postdoc research with Peter Wainwright and Shaun Collin. Early on we recognized that comparisons between different eyes (be it of the same species or eyes from different species) wasn’t necessarily straightforward. Two major problems emerged: (1) the incisions required to flatten the eye cup in order to make a wholemount were never quite consistent; and (2) the reconstruction of topography, often done by manual interpolation, didn’t seem 100% accurate or objective. Obviously we weren’t the first to notice this. I’m not going to review the entire body of literature (we tried to do this as thoroughly as possible in the paper, but I want to highlight two recent contributions by David Sterratt and Eduardo Garza-Gisholt.

‘Retina’ is very easy to learn, and with stereology count data at hand, you can generate several maps per hour. Useful features include generation of average maps and a range of descriptive statistics that allow for a deeper assessment of the modeled map. An extensive tutorial with example data, and, of course, all code, is available on Github. If you would like more detailed instructions on how to use the software, please do not hesitate to contact us.

If you are planning on working on retinal maps in the future, it would be great if you gave our software a try. We hope it will be useful! There are many aspects of quantitative retinal mapping that are understudied and any additional empirical study will be very helpful in moving our field forward. Please also let us know if you have any questions, concerns, and suggestions. Our goal is to further develop Retina based on feedback and requests from users.

Specifically, what criteria are important for you when making retinal topography maps?

What features of the current version do you like (or dislike)?

We would love to hear from you.

]]>Retinal topography mapecomorphFigure 1. An example of the functionality of Retiina. Panel (a) shows a simplified outline and the sampling locations of a retinal wholemount. Panel (b) shows the reconstructed map, while (c) illustrates the fit error of the model. [Figure 1 of Cohn et al. 2015, Journal of Vision]